Introduction
The family Lumbrineridae Schmarda, 1861 (Annelida) has received renewed attention during the last two decades, mostly thanks to the efforts of Luis Fernando Carrera-Parra and collaborators, who have reviewed totally or partially some of its genera, such as Cenogenus Chamberlin, 1919 (Carrera-Parra 2001b), Kuwaita Mohammad, 1973 (Carrera-Parra and Orensanz 2002), Lumbricalus Frame, 1992 (Carrera-Parra 2004), and Lumbrineris de Blainville, 1828 (Carrera-Parra 2006b), occasionally with the support of phylogenetic analyses (Carrera-Parra 2005, 2006a). More recently, the first partial revision of Lumbrineridae based on molecular data confirmed the monophyly of Abyssoninoe Orensanz, 1990, Augeneria Monro, 1930, Gallardoneris Carrera-Parra, 2006, Lumbrineriopsis Orensanz, 1973 and Ninoe Kinberg, 1865, while Helmutneris Carrera-Parra, 2006, Hilbigneris Carrera-Parra, 2006 and Lumbrinerides Orensanz, 1973 were recovered as independent genera, and Lumbrineris and Scoletoma de Blainville, 1828 were considered polyphyletic (Borisova and Budaeva 2022).
The studies by Carrera-Parra and co-authors also triggered numerous collaborations dealing with local faunas, some of them covering the waters of the Iberian Peninsula (Martins et al. 2012; Arias and Carrera-Parra 2014; García Gómez et al. 2016) or the Mediterranean Sea (Carrera-Parra et al. 2011; Katsiaras et al. 2018). These, combined with other studies (Gil 2011; Bertasi et al. 2014; D’Alessandro et al. 2014; D’Alessandro et al. 2016; Kurt-Sahin et al. 2016; Aguirrezabalaga and Arias 2018; Langeneck et al. 2020), reported ~ 35 lumbrinerid species for the Iberian Atlanto-Mediterranean waters and ~ 30 for the whole Mediterranean Sea, belonging to the genera Abyssoninoe, Augeneria, Cenogenus, Eranno Kinberg, 1865, Gallardoneris, Helmutneris, Hilbigneris, Kuwaita, Lumbricalus, Lumbrinerides, Lumbrineriopsis, Lumbrineris, Ninoe, and Scoletoma.
Among them, Gallardoneris was first described to include two Indo-Pacific species, G. shiinoi (Gallardo, 1968), from Vietnam, and G. thailandensis Carrera-Parra, 2006, from Thailand (Carrera-Parra 2006a). More recently, Gallardoneris iberica Martins, Carrera-Parra, Quintino & Rodrigues, 2012 was described from Portuguese waters (Iberian Peninsula, NE Atlantic) as being the third species of the genus (Martins et al. 2012). Shortly after it was reported from Italy (Bertasi et al. 2014; D’Alessandro et al. 2016), the Spanish Atlanto-Mediterranean coasts of the Iberian Peninsula (García Gómez et al. 2016), Greece and Cyprus (Katsiaras et al. 2018).
Through the analysis of numerous specimens from multiple surveys in the western Mediterranean Sea (but mainly in Spanish and French waters), we realised that those usually identified as Lumbrineris nonatoi Ramos, 1976, a species originally described from the western Mediterranean, fitted perfectly with the description of the newly reported G. iberica. Lumbrineris nonatoi had been commonly recorded in that sector from shallow shelf soft sediments for more than 30 years, and had also been widely reported across the whole Mediterranean Sea from areas such as the Gulf of Lions (Labrune et al. 2007), Italian waters (Castelli et al. 1995), Adriatic Sea (Mikac 2015), Crete (Papadopoulou et al. 1994), Cyprus (Çinar 2005), or Turkey (Çinar and Dagli 2013). However, it stopped being reported after the description of G. iberica by Martins et al. (2012).
As part of his taxonomic works on lumbrinerids, Carrera-Parra (2001a, 2006b) provided a redescription of L. nonatoi. In the absence of more suitable material, this redescription was based on specimens from the Gulf of Mexico, while the original description corresponded to specimens from the Catalan Sea (western Mediterranean) (Ramos 1976). As a result, L. nonatoi was retained in Lumbrineris (Carrera-Parra 2001a, 2006b) and, as such, joined other species of the genus in recent identification keys for the Mediterranean and southwest European Atlantic waters (Martins et al. 2012; D’Alessandro et al. 2016; García Gómez et al. 2016; Aguirrezabalaga and Arias 2018). Considering the reported characters, however, it is now clear that the redescription and the original description refer to different species, with the Mexican specimens belonging to Lumbrineris, as currently defined (Carrera-Parra 2006a).
Four consequences derive from this misidentification. First, the recently described G. iberica should be considered a junior synonym of L. nonatoi sensu Ramos (1976) and, thus, all successive citations of the former from European Atlanto-Mediterranean waters should presumably be assigned to the latter (e.g., Martins et al. 2012; Bertasi et al. 2014; D’Alessandro et al. 2016; García Gómez et al. 2016; Aguirrezabalaga and Arias 2018; Katsiaras et al. 2018). Second, according to the generic diagnostic characters described by Carrera-Parra (2006b), the European L. nonatoi clearly represents a species of Gallardoneris. Third, no European lumbrinerid can be correctly identified as “Lumbrineris nonatoi” using the most recent literature for the region, which either refers to the misidentified specimens from the Gulf of Mexico (not present in European waters), or to a chimera composed of characters from the specimens of the Gulf of Mexico mixed with features from the original description of L. nonatoi. Fourth, the specimens from the Gulf of Mexico attributed to “Lumbrineris nonatoi” by Carrera-Parra (2001a; 2006b) belong instead to a new species.
Materials and methods
Numerous specimens of Lumbrineris nonatoi sensu Ramos (1976) collected from the Mediterranean coasts of Spain and France, were studied and used to confirm the accurate original description by Ramos (1976). A selection of 40 entire specimens from the French Mediterranean coasts were used for morphometric measurements of body length and width, prostomium and peristomium length and width, length and width at chaetigers 10 and 15, total number of chaetigers, and number of chaetigers with composite hooks and bilimbate chaetae. The relationships between the quantitative characters measured were estimated by linear regression and plotted using the statistical software XLSTAT 2015 (Addinsoft).
Denotation of maxillary elements follows Carrera-Parra (2006a) and Martins et al. (2012) and, thus, MI–MIV corresponds to maxillae I to IV. Other abbreviations in the text are: CMHH = composite hooded hooks; D1–D2 = first and second teeth pair, according to Ramos (1976); L = length; N = number of examined specimens; p = significance level (probability); post: postchaetal lobe; pre: prechaetal lobe; R2 = Square Pearson coefficient; SMHH = simple hooded hooks; W = width.
Representative specimens of Lumbrineris nonatoi sensu Ramos (1976) are deposited in the collections of the Centre for Advanced Studies of Blanes (CEAB) of the High Council for Scientific Research (CSIC, Spain). Type and non-type materials of G. iberica were loaned from the Biological Research Collection of Marine Invertebrates (COBI) of the Biology Department of the University of Aveiro (Portugal).
The Mexican specimens of Lumbrineris nonatoi sensu Carrera-Parra (2001a; 2006b) are here described as a new species. The description is provided in accordance with article 72.4.2 of the International Code of Zoological Nomenclature (International Commission on Zoological Nomenclature 1999), concerning new nominal species-group taxa being based on a published misidentification by an earlier author. While we did not follow recommendation 73B of the Code (International Commission on Zoological Nomenclature 1999) in that “An author should designate as holotype a specimen actually studied by him or her, not a specimen known to the author only from descriptions or illustrations in the literature”, the materials were perfectly and accurately described by Carrera-Parra (2001a, 2006b). Therefore, no additional observations of new materials or samples were found to be necessary. The holotype and paratypes of the new species were selected with the assistance of Dr Carrera-Parra among the specimens deposited in the Reference Collection of Benthos of ECOSUR-Chetumal, Mexico (ECOSUR), in the Colección de Poliquetos del Instituto de Ciencias del Mar y Limnología, UNAM, Mexico (CP-ICML-UNAM), and in the National Museum of Natural History, Smithsonian Institution, Washington D.C., USA (USNM). Additional information concerning the types was retrieved from Uebelacker (1984), Carrera-Parra (2001a, 2006b), and GBIF Secretariat (2021).
The electronic version of this article in portable document format (PDF) will represent a published work according to the ICZN (International Commission on Zoological Nomenclature 1999), and hence the new names contained in the electronic version are effectively published under that Code from the electronic edition alone.
Discussion
Lumbrineris nonatoi vs. Gallardoneris nonatoi
The origin of the misconception leading to the description of G. iberica and its successive records across the European Atlanto-Mediterranean waters seems to be clear. It lays mainly in the redescription of “Lumbrineris nonatoi” based on specimens collected from the Gulf of Mexico (Carrera-Parra 2001a, 2006b), which inadvertently introduced a misidentification for the European L. nonatoi. A more suitable approach to the supposed lack of type material would have been to rely on the original description of L. nonatoi by Ramos (1976), complementing it with new material from the type locality or nearby Mediterranean waters. The misidentified Mexican Gulf specimens used to redescribe “Lumbrineris nonatoi” showed five pairs of maxillae, thus justifying being assigned to Lumbrineris (Carrera-Parra 2001a, 2006b), while the specimens used in the original description showed only four (Ramos 1976), allowing it to be placed in Gallardoneris.
It should be considered that species descriptions of Lumbrineris and other lumbrinerids previous to the 1970s habitually did not report maxillae V. This structure was generally not recognized as a maxilla, but rather referred to as a lateral element or a lateral support, if mentioned at all. This was also the case with Ramos (1976), who counted four pairs of maxillae for all species of Lumbrineris she described (as MI, MII, D1, D2), while variously reporting accessory elements. Accordingly, Carrera-Parra (2001a, 2006b) may have assumed that maxillae V were present in the Mediterranean specimens of L. nonatoi sensu Ramos (1976), but not mentioned in the description.
The genus Gallardoneris was considered as monophyletic by Borisova and Budaeva (2022). However, these authors also stated that the specimens used in their analysis, provisionally identified as G. iberica and collected from western African Atlantic waters (i.e., two from Morocco, one from Mauritania and one from Senegal) showed a similar morphology, but clearly diverged molecularly. Accordingly, Borisova and Budaeva (2022) suggested the possible existence of a cryptic complex within the genus that would require further analyses based on a larger number of specimens. Despite we agree with the necessity of further studies, at present this does not contradict the fact that the comparison of the original descriptions of G. iberica by Martins et al. (2012) and L. nonatoi by Ramos (1976) supports they are the same species. Actually, based on the current knowledge, two aspects sustain the synonymy here proposed. First, the fact that our results are supported by the conclusions of Bertasi et al. (2014) and García Gómez et al. (2016), who compared Mediterranean specimens of Gallardoneris with types of G. iberica and also concluded that they represented one single species, herein identified as G. nonatoi comb. nov. Second, the lack of detailed morphological information on the West African specimens tentatively attributed to G. iberica by Borisova and Budaeva (2022) (e.g., there are no data on the presence or number of anal cirri) and the lack of molecular information on the Portuguese and Mediterranean specimens, which does not allow any comparison.
Consequently, the previously reported presence of Gallardoneris in European waters (Martins et al. 2012; Bertasi et al. 2014; D’Alessandro et al. 2016; García Gómez et al. 2016; Aguirrezabalaga and Arias 2018; Katsiaras et al. 2018) is here confirmed, but the species representing the genus is, in fact, G. nonatoi comb. nov., with G. iberica being a junior synonym. Accordingly, the misidentified Mexican Gulf specimens attributed to L. nonatoi by Carrera-Parra (2006b) clearly represent a different taxon, which turns out to be a new species that we have named L. jan sp. nov.
By clarifying the taxonomic situation of G. nonatoi comb. nov., we are also explaining the existence of very numerous Mediterranean reports of L. nonatoi previous to the publication of Martins et al. (2012), in contrast to an apparent disappearance of the species in the whole area and its replacement by a proliferation of G. iberica (see Bertasi et al. 2014; Katsiaras et al. 2018 and references herein), together with new records of “Lumbrineris nonatoi” in the Gulf of Mexico. By defining the new species and proposing the new combination, we also contribute to solving possible doubts concerning the origin, population fluctuations, and colonization dynamics of the species involved. We are thus showing that the two names represent one single species in European waters, different from the one from the Gulf of Mexico. In light of our observations, their respective distributions remain restricted to their own (original) geographical areas, from where there is no reason to assume they are not native. Therefore, considering the present knowledge, there is no room for discussion of possible introductions or invasions, nor for incorporation of new names to the already growing lists of alien species.
On other possible Mediterranean species of Gallardoneris
In addition to “Lumbrineris nonatoi”, there is another species deserving to be mentioned in the context of our study. Lumbrineris longipodiata Cantone, 1990 was described from specimens of the Gulf of Catania (Mediterranean Sea), collected in fine sands between 14–16 m depth (Cantone 1990). This is a poorly known species that has been seldom recorded since its short and incomplete (by today’s standards) original description. Though, it could represent an additional member of Gallardoneris. The original description reported only four pairs of maxillae, carriers as long as MI, simple and composite multidentate hooded hooks (the latter with short blades), and absence of antennae and branchiae. However, despite some details on the maxillary apparatus were not available, its carriers did not seem to join the entire base of MI and its mandibles were completely fused only along 2/3 of its length, which prevents us to allocate the species in the genus with certainty. Moreover, the identification of further specimens of L. longipodiata is eventually hampered by being erroneously keyed with five pairs of maxillae (and so placed within Lumbrineris) in the keys available for the region (e.g., Gil 2011; D’Alessandro et al. 2016). A level of confusion still increased by D’Alessandro et al. (2016) further keying out L. longipodiata as having bidentate composite hooded hooks, when they are absent in this species. Conversely, it was described as having only four maxillae and thus it should be keyed near to, or even within, Gallardoneris. However, many lumbrinerid descriptions lacked information about the presence of MV, which could also be the case with the original description of L. longipodiata. Certainly this is critical information that needs to be corroborated.
Lumbrineris longipodiata resembles G. nonatoi comb. nov. in having the prechaetal lobe poorly developed and smaller than the postchaetal one in the first chaetigers, of similar size around chaetiger 25 and slightly longer from chaetiger 110, with both lobes becoming cirriform, to twice longer in the last segments. However, it differs in having bidentate MIII, composite hooks to ca. chaetiger 19, and pygidium with two anal cirri (vs. edentate MIII, to ca. chaetiger 9, and anal cirri absent in G. nonatoi comb. nov., respectively). Particularly, the differences in mandible shape, fused only in 2/3 of its length in L. longipodiata and completely fused in the species of Gallardoneris cast additional doubts on its assignment to that genus. The presence of only two anal cirri (also recorded in L. jan sp. nov.) is a rare feature among lumbrinerids, being considered as distinctive of L. longipodiata (Cantone 1990). Still, despite the number of anal cirri is frequently a size-dependent character (Frame 1992), its single presence (no matter how many) separates clearly L. longipodiata from G. nonatoi comb. nov., which lacks them. Therefore, in spite of the above-mentioned similarities, the two taxa do not seem to represent the same species. Considering all aspects discussed above, we conclude that it is necessary to redescribe L. longipodiata based on topotypic specimens before being able to make a convincing decision on its taxonomic status.
Clearly the knowledge on the European lumbrinerid fauna, especially in the supposedly well-studied Mediterranean Sea, is far from being fully accomplished. Several taxonomic problems remain open, the status of many ancient species has not been revised for decades, and the validity of some of them was never reassessed since their original description or first synonymy, while new names have been introduced for taxa occurring in the same localities. Other records refer to species originally described from distant biogeographic areas and very unlikely occurring in the region. While their records resulted probably from misidentifications derived from the use of bibliography unsuitable to identify the local fauna, they have now entered the local lists of presumed alien and/or introduced species (Langeneck et al. 2020; DM and JG, unpublished data). Definitely, the number of species occurring in the area will keep swinging, especially considering that the acceptance or the rejection of some of them will surely not be consensual among specialists.